Analysis of protein covalent modification by xenobiotics using a covert oxidatively activated tag: Raloxifene proof-of-principle study

Chemical Research in Toxicology

Volumn 18, Issue 9, 2005, Pages 1485-1496

  Liu, Ju ^a   Li, Qian ^a   Yang, Xiaofeng ^a   Van Breemen, Richard B ^a   Bolton, Judy L ^a   Thatcher, Gregory R J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTIN; CELL PROTEIN; CYTOSOLIC GLUCOSE REGULATED PROTEIN; GLUTATHIONE TRANSFERASE; IODOACETAMIDE; ISOMERASE; PHENOL DERIVATIVE; POLYCYCLIC AROMATIC HYDROCARBON; PROTEIN DISULFIDE ISOMERASE; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; CHEMOPROPHYLAXIS; CONTROLLED STUDY; COVALENT BOND; CYTOTOXICITY; MENOPAUSAL SYNDROME; NONHUMAN; NUCLEIC ACID ANALYSIS; OXIDATION REDUCTION REACTION; OXIDATIVELY ACTIVATED TAG; PROTEIN ANALYSIS; PROTEIN MODIFICATION; QUANTITATIVE DIAGNOSIS; RAT; XENOBIOTIC METABOLISM;

ANIMALS; HUMANS; MASS SPECTROMETRY; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; PROTEINS; RALOXIFENE; RATS; XENOBIOTICS;

EID: 25444462779     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx0501738     Document Type: Article

References (56)

1. Rossouw, J. E., Anderson, G. L., Prentice, R. L., LaCroix, A. Z., Kooperberg, C., Stefanick, M. L., Jackson, R. D., Beresford, S. A., Howard, B. V., Johnson, K. C., Kotchen, J. M., and Ockene, J. (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: Principal results From the Women's Health Initiative randomized controlled trial. J. Am. Med. Assoc. 288, 321-333.
2. Delmas, P. D., Bjarnason, N. H., Mitlak, B. H., Ravoux, A. C., Shah, A. S., Huster, W. J., Draper, M., and Christiansen, C. (1997) Effects of raloxifene on bone mineral density, serum cholesterol concentrations, and uterine endometrium in postmenopausal women. N. Engl. J. Med. 337, 1641-1647.
3. Fisher, B., Costantino, J. P., Wickerham, D. L., Redmond, C. K., Kavanah, M., Cronin, W. M., Vogel, V., Robidoux, A., Dimitrov, N., Atkins, J., Daly, M., Wieand, S., Tan-Chiu, E., Ford, L., and Wolmark, N. (1998) Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J. Natl. Cancer Inst. 90, 1371-1388.
4. King, C. M. (1995) Tamoxifen and the induction of cancer. Carcinogenesis 16, 1449-1454.
5. van Leeuwen, F. E., Benraadt, J., Coebergh, J. W., Kiemeney, L. A., Gimbráere, C. H., Otter, R., Schouten, L. J., Damhuis, R. A., Bontenbal, M., and Diepenhorst, F. W., et al. (1994) Risk of endometrial cancer after tamoxifen treatment of breast cancer. Lancet 343, 448-452.
6. Zhang, F., Fan, P. W., Liu, X., Shen, L., van Breemen, R. B., and Bolton, J. L. (2000) Synthesis and reactivity of a potential carcinogenic metabolite of tamoxifen: 3,4-Dihydroxytamoxifen-o-quinone. Chem. Res. Toxicol. 13, 53-62.
7. Shibutani, S., Ravindernath, A., Suzuki, N., Terashima, L., Sugarman, S. M., Grollman, A. P., and Pearl, M. L. (2000) Identification of tamoxifen-DNA adducts in the endometrium of women treated with tamoxifen. Carcinogenesis 21, 1461-1467.
8. Yu, L., Liu, H., Li, W., Zhang, F., Luckie, C., van Breemen, R. B., Thatcher, G. R. J., and Bolton, J. L. (2004) Oxidation of raloxifene to quinoids: Potential toxic pathways via a diquinone methide and o-quinones. Chem. Res. Toxicol. 17, 879-888.
9. Shen, L., Pisha, E., Huang, Z., Pezzuto, J. M., Krol, E., Alam, Z., van Breemen, R. B., and Bolton, J. L. (1997) Bioreductive activation of catechol estrogen-ortho-quinones: Aromatization of the B ring in 4-hydroxyequilenin markedly alters quinoid formation and reactivity. Carcinogenesis 18, 1093-1101.
10. Han, X., and Liehr, J. G. (1995) Microsome-mediated 8-hydroxylation of guanine bases of DNA by steroid estrogens: correlation of DNA damage by free radicals with metabolic activation to quinones. Carcinogenesis 16, 2571-2574.
11. Liu, J., Liu, H., van Breemen, R. B., Thatcher, G. R. J., and Bolton, J. L. (2005) Bioactivation of the selective estrogen receptor modulator acolbifene to quinone methides. Chem. Res. Toxicol. 18, 174-182.
12. Liu, H., Liu, J., van Breemen, R. B., Thatcher, G. R. J., and Bolton, J. L. (2005) Bioactivation of the selective estrogen receptor modulator desmethylated arzoxifene to quinoids: 4′-fluoro substitution prevents quinoid formation. Chem. Res. Toxicol. 18, 162-173.
13. Chen, Q., Ngui, J. S., Doss, G. A., Wang, R. W., Cai, X., DiNinno, F. P., Blizzard, T. A., Hammond, M. L., Stearns, R. A., Evans, D. C., Baillie, T. A., and Tang, W. (2002) Cytochrome P450 3A4-mediated bioactivation of raloxifene: irreversible enzyme inhibition and thiol adduct formation. Chem. Res. Toxicol. 15, 907-914.
14. Bateman, K. P., Baker, J., Wilke, M., Lee, J., Leriche, T., Seto, C., Day, S., Chauret, N., Quellet, M., and Nicoll-Griffith, D. A. (2004) Detection of covalent adducts to cytochrome P450 3A4 using liquid chromatography mass spectrometry. Chem. Res. Toxicol. 17, 1356-1361.
15. Zhou, S., Chan, E., Duan, W., Huang, M., and Chen, Y. Z. (2005) Drug bioactivation, covalent binding to target proteins and toxicity relevance. Drug Metab. Rev. 37, 41-213.
16. Kim, J. R., Yoon, H. W., Kwon, K. S., Lee, S. R., and Rhee, S. G. (2000) Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH. Anal. Biochem. 283, 214-221.
17. Evans, D. C., Watt, A. P., Nicoll-Griffith, D. A., and Baillie, T. A. (2004) Drug-protein adducts: An industry perspective on minimizing the potential for drug bioactivation in drug discovery and development. Chem. Res. Toxicol. 17, 3-16.
18. Cohen, S. D., Pumford, N. R., Khairallah, E. A., Boekelheide, K., Pohl, L. R., Amouzadeh, H. R., and Hinson, J. A. (1997) Selective protein covalent binding and target organ toxicity. Toxicol. Appl. Pharmacol. 143, 1-12.
19. Wakabayashi, N., Dinkova-Kostova, A. T., Holtzclaw, W. D., Kang, M. I., Kobayashi, A., Yamamoto, M., Kensler, T. W., and Talalay, P. (2004) Protection against electrophile and oxidant stress by induction of the phase 2 response: Fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl. Acad. Sci. U.S.A. 101, 2040-2045.
20. Chang, M., Bolton, J. L., and Blond, S. Y. (1999) Expression and purification of hexahistidine-tagged human glutathione S-transferase P1-1 in Escherichia coli. Protein Expression Purif. 17, 443-448.
21. Chevalier, M., King, L., and Blond, S. (1998) Purification and properties of BiP. Methods Enzymol. 290, 384-409.
22. Ji, Y., Toader, V., and Bennett, B. M. (2002) Regulation of microsomal and cytosolic glutathione S-transferase activities by S-nitrosylation. Biochem. Pharmacol. 63, 1397-1404.
23. Thompson, J. A., Malkinson, A. M., Wand, M. D., Mastovich, S. L., Mead, E. W., Schullek, K. M., and Laudenschlager, W. G. (1987) Oxidative metabolism of butylated hydroxytoluene by hepatic and pulmonary microsomes from rats and mice. Drug Metab. Dispos. 15, 833-840.
24. Landry, F., Lombardo, C. R., and Smith, J. W. (2000) A method for application of samples to matrix-assisted laser desorption ionization time-of-flight targets that enhances peptide detection. Anal. Biochem. 279, 1-8.
25. Nishihira, J., Ishibashi, T., Sakai, M., Nishi, S., Kumazaki, T., Hatanaka, Y., Tsuda, S., and Hikichi, K. (1992) Characterization of cysteine residues of glutathione S-transferase P: Evidence for steric hindrance of substrate binding by a bulky adduct to cysteine 47. Biochem. Biophys. Res. Commun. 188, 424-432.
26. Lo Bello, M., Petruzzelli, R., De Stefano, E., Tenedini, C., Barra, D., and Federici, G. (1990) Identification of a highly reactive sulphydryl group in human placental glutathione transferase by a site-directed fluorescent reagent. FEBS Lett. 263, 389-391.
27. Chang, M., Shin, Y. G., van Breemen, R. B., Blond, S. Y., and Bolton, J. L. (2001) Structural and functional consequences of inactivation of human glutathione S-transferase P1-1 mediated by the catechol metabolite of equine estrogens, 4-hydroxyequilenin. Biochemistry 40, 4811-4820.
28. Hemminki, K., Rajaniemi, H., Lindahl, B., and Moberger, B. (1996) Tamoxifen-induced DNA adducts in endometrial samples from breast cancer patients. Cancer Res. 56, 4374-4377.
29. Fan, P. W., Zhang, F., and Bolton, J. L. (2000) 4-Hydroxylated metabolites of the antiestrogens tamoxifen and toremifene are metabolized to unusually stable quinone methides. Chem. Res. Toxicol. 13, 45-52.
30. Zhang, F., Chen, Y., Pisha, E., Shen, L., Xiong, Y., van Breemen, R. B., and Bolton, J. L. (1999) The major metabolite of equilin, 4-hydroxyequilin, autoxidizes to an o-quinone which isomerizes to the potent cytotoxin 4-hydroxyequilenin-o-quinone. Chem. Res. Toxicol. 12, 204-213.
31. Bolton, J. L., Yu, L., and Thatcher, G. R. J. (2004) Quinoids formed from estrogens and antiestrogens. Methods Enzymol. 378, 110-123.
32. Dehal, S. S., and Kupfer, D. (1999) Cytochrome P-450 3A and 2D6 catalyze ortho hydroxylation of 4-hydroxytamoxifen and 3-hydroxytamoxifen (droloxifene) yielding tamoxifen catechol: Involvement of catechols in covalent binding to hepatic proteins. Drug Metab. Dispos. 27, 681-688.
33. Mani, C., and Kupfer, D. (1991) Cytochrome P-450-mediated activation and irreversible binding of the antiestrogen tamoxifen to proteins in rat and human liver: Possible involvement of flavin-containing monooxygenases in tamoxifen activation. Cancer Res. 51, 6052-6058.
34. Kumar, S., Zhou, B., Liang, F., Wang, W. Q., Huang, Z., and Zhang, Z. Y. (2004) Activity-based probes for protein tyrosine phosphatases. Proc. Natl. Acad. Sci. U.S.A. 101, 7943-7948.
35. Kidd, D., Liu, Y., and Cravatt, B. F. (2001) Profiling serine hydrolase activities in complex proteomes. Biochemistry 40, 4005-4015.
36. Mitra, K., Marquis, J. C., Hillier, S. M., Rye, P. T., Zayas, B., Lee, A. S., Essigmann, J. M., and Croy, R. G. (2002) A rationally designed genotoxin that selectively destroys estrogen receptor-positive breast cancer cells. J. Am. Chem. Soc. 124, 1862-1863.
37. Graf, R., and Friedl, P. (1999) Detection of immobilized proteins on nitrocellulose membranes using a biotinylation-dependent system. Anal. Biochem. 273, 291-297.
38. Suh, S. K., Hood, B. L., Kim, B. J., Conrads, T. P., Veenstra, T. D., and Song, B. J. (2004) Identification of oxidized mitochondrial proteins in alcohol-exposed human hepatoma cells and mouse liver. Proteomics 4, 3401-3412.
39. Prestera, T., Holtzclaw, W. D., Zhang, Y., and Talalay, P. (1993) Chemical and molecular regulation of enzymes that detoxify carcinogens. Proc. Natl. Acad. Sci. U.S.A. 90, 2965-2969.
40. Yu, L., Liu, H., Li, W., Zhang, F., Luckie, C., Van Breemen, R. B., Thatcher, G. R. J., and Bolton, J. L. (2004) Oxidation of raloxifene to quinoids: potential toxic pathways via a diquinone methide and o-quinones. Chem. Res. Toxicol. 17, 879-888.
41. Toader, V., Xu, X., Nicolescu, A., Yu, L., Bolton, J. L., and Thatcher, G. R. J. (2003) Nitrosation, nitration, and autoxidation of the selective estrogen receptor modulator raloxifene by nitric oxide, peroxynitrite, and reactive nitrogen/oxygen species. Chem. Res. Toxicol. 16, 1264-1276.
42. Koen, Y. M., and Hanzlik, R. P. (2002) Identification of seven proteins in the endoplasmic reticulum as targets for reactive metabolites of bromobenzene. Chem. Res. Toxicol. 15, 699-706.
43. Ferrari, D. M., and Sèoling, H. D. (1999) The protein disulphide-isomerase family: Unravelling a string of folds. Biochem. J. 339, 1-10.
44. Zhou, L., McKenzie, B. A., Eccleston, E. D., Jr., Srivastava, S. P., Chen, N., Erickson, R. R., and Holtzman, J. L. (1996) The covalent binding of [14C]acetaminophen to mouse hepatic microsomal proteins: The specific binding to calreticulin and the two forms of the thiol:protein disulfide oxidoreductases. Chem. Res. Toxicol. 9, 1176-1182.
45. Zhou, L. X., Dehal, S. S., Kupfer, D., Morrell, S., McKenzie, B. A., Eccleston, E. D., Jr., and Holtzman, J. L. (1995) Cytochrome P450 catalyzed covalent binding of methoxychlor to rat hepatic, microsomal iodothyronine 5′-monodeiodinase, type I: Does exposure to methoxychlor disrupt thyroid hormone metabolism? Arch. Biochem. Biophys. 322, 390-394.
46. Haas, I. G. (1994) BiP (GRP78), an essential hsp70 resident protein in the endoplasmic reticulum. Experientia 50, 1012-1120.
47. Barnes, J. A., Smoak, I. W., and Branch, S. (1999) Expression of glucose-regulated proteins (GRP78 and GRP94) in hearts and fore-limb buds of mouse embryos exposed to hypoglycemia in vitro. Cell Stress Chaperones 4, 250-258.
48. Katayama, T., Imaizumi, K., Sato, N., Miyoshi, K., Kudo, T., Hitomi, J., Morihara, T., Yoneda, T., Gomi, F., Mori, Y., Nakano, Y., Takeda, J., Tsuda, T., Itoyama, Y., Murayama, O., Takashima, A., St. George-Hyslop, P., Takeda, M., and Tohyama, M. (1999) Presenilin-1 mutations downregulate the signaling pathway of the unfolded-protein response. Nat. Cell Biol. 1, 479-485.
49. Koomèagi, R., Mattern, J., and Volm, M. (1999) Glucose-related protein (GRP78) and its relationship to the drug-resistance proteins P170, GST-pi, LRP56 and angiogenesis in nonsmall cell lung carcinomas. Anticancer Res. 19, 4333-4336.
50. Freedman, R. B., Hirst, T. R., and Tuite, M. F. (1994) Protein disulphide isomerase: Building bridges in protein folding. Trends Biochem. Sci. 19, 331-336.
51. Hawkins, H. C., and Freedman, R. B. (1991) The reactivities and ionization properties of the active-site dithiol groups of mammalian protein disulphide-isomerase. Biochem. J. 275, 335-339.
52. Bennett, C. F., Balcarek, J. M., Varrichio, A., and Crooke, S. T. (1988) Molecular cloning and complete amino acid sequence of form-I phosphoinositide-specific phospholipase C. Nature 334, 268-270.
53. Fan, P. W., Zhang, F., and Bolton, J. L. (2000) 4-Hydroxylated metabolites of the antiestrogens tamoxifen and toremifene are metabolized to unusually stable quinone methides. Chem. Res. Toxicol. 13, 45-52.
54. Thompson, D. C., Perera, K., Krol, E. S., and Bolton, J. L. (1995) o-Methoxy-4-alkylphenols that form quinone methides of intermediate reactivity are the most toxic in rat liver slices. Chem. Res. Toxicol. 8, 323-327.
55. Amouzadeh, H. R., Bourdi, M., Martin, J. L., Martin, B. M., and Pohl, L. R. (1997) UDP-glucose:glycoprotein glucosyltransferase associates with endoplasmic reticulum chaperones and its activity is decreased in vivo by the inhalation anesthetic halothane. Chem. Res. Toxicol. 10, 59-63.
56. Kwak, M. K., Wakabayashi, N., and Kensler, T. W. (2004) Chemoprevention through the Keapl-Nrf2 signaling pathway by phase 2 enzyme inducers. Mutat. Res. 555, 133-148.